Bacteria foster fast fruit fly fornication preference changes

A single generation of fruit flies on a new food source can alter their mating …

People tend to focus on Darwin's ideas about natural selection, but he also spent a portion of The Origin of Species discussing another powerful evolutionary force: sexual selection. If a species prefers to mate with members that have a specific trait—bright plumage, for example—it won't take long for that trait to sweep through the species. In the same way, having two different mating preferences in a single population can split it in two in the same way that a geographic barrier can. In both cases, geography and mate choice, the resulting reproductive isolation can ultimately lead to the evolution of new species, as each population undergoes separate genetic changes. This week, PNAS published a paper showing that this sort of reproductive isolation can take as little as a single generation in flies, because it doesn't rely on genetic changes in the insects—it's driven by the bacteria that live on them.

This sort of reproductive isolation isn't just theory; it's been demonstrated in the lab. Fruit flies can be grown under different conditions—temperature, humidity, food source—for multiple generations, after which the flies will have a strong preference for mating with those raised under identical conditions. Even when the flies are no longer isolated, they mate as if they were.

The new experiments seemed to have started out as if they were heading in the same direction. A single population of flies was split, and separate groups were reared on two different food sources, one sugar-based, the other starch. After 25 generations, the two groups had a strong preference for mating with their peers from the same food source. So far, perfectly normal. Things started to get weird when the authors started testing earlier generations, though. The mating preference was already present at 11 generations and, shockingly, also appeared at the second generation, way too fast for a genetic change to sweep through the population.

With genetics ruled out, an environmental factor was the obvious choice, and the authors decided to look into whether bacteria in the different food sources made a difference. Treating the flies with antibiotics completely wiped out the mating preference, confirming their suspicions. So, they sampled the bacteria present in the two different populations, and found a single species, the starch-loving Lactobacillus plantarum, that was present in far higher numbers in one of the two populations. So, they treated the flies with antibiotics to get rid of the resident bacteria, and then inoculated them with L. plantarum. This created a mating preference as well.

How could a bacterial species have this effect? The authors think it's all in the pheromones flies use for mating. These are released from the fly's cuticle, where the bacteria take up residence. Their presence then alters the relative amounts of several of these pheromones, tweaking the sexual signals sent out by the flies.

The findings provide some experimental support for a relatively new idea about evolutionary selection. Since Darwin's time we've tended to assume that items under selection are the genes carried by an organism or population of organisms. But these results show that it's not just a host's genome that can undergo selection; it's the host plus everything that lives on or in it. The Hologenome Theory posits that it's the host genome plus its associated microorganisms that ends up being the unit of selection.

At this point, it's probably worth noting that every one of us carries far more copies of bacterial genomes than we do of our own, human genome.